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. 2015 Sep 11;1(8):e1500363.
doi: 10.1126/sciadv.1500363. eCollection 2015 Sep.

The energetic cost of vision and the evolution of eyeless Mexican cavefish

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The energetic cost of vision and the evolution of eyeless Mexican cavefish

Damian Moran et al. Sci Adv. .

Abstract

One hypothesis for the reduction of vision in cave animals, such as the eyeless Mexican cavefish, is the high energetic cost of neural tissue and low food availability in subterranean habitats. However, data on relative brain and eye mass in this species or on any measure of the energetic cost of neural tissue are not available, making it difficult to evaluate the "expensive tissue hypothesis." We show that the eyes and optic tectum represent significant metabolic costs in the eyed phenotype. The cost of vision was calculated to be 15% of resting metabolism for a 1-g fish, decreasing to 5% in an 8.5-g fish as relative eye and brain size declined during growth. Our results demonstrate that the loss of the visual system in the cave phenotype substantially lowered the amount of energy expended on expensive neural tissue during diversification into subterranean rivers, in particular for juvenile fish.

Keywords: Biology; Brain Evolution; Cave; Eye Evolution; Physiological Energetics; Subterranean.

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Figures

Fig. 1
Fig. 1. A comparison of brain size and body morphology in the four Mexican tetra morphs used in this study.
Scale bars are approximate.
Fig. 2
Fig. 2. Brain and eye mass allometry in the four Mexican tetra morphs.
(A) Eye mass (percentage of body weight) versus total body weight. (B) Brain mass (percentage of body weight) versus total body weight. (C) Dependence of brain mass on eye mass among eyed morphs.
Fig. 3
Fig. 3. Summary graphs of respirometry data showing the oxygen consumption rates of eyes and brains in surface and Pachón ecotypes at different times of day.
Each gray line represents a single organ measurement. A running mean ± 95% confidence interval is overlaid.
Fig. 4
Fig. 4. Output from a model used to calculate the relative energetic costs of eyes, brain, and vision for three Mexican tetra ecotypes.
(A) Whole body oxygen consumption (B) relative brain size (C) brain oxygen consumption (D) relative eye size (E) oxygen consumption of eyes (F) oxygen consumption of eyes plus brain (G) oxygen consumption of eyes plus optic tectum. Refer to the Supplementary Materials for the calculative approach.
Fig. 5
Fig. 5. A schematic drawing of the respirometry apparatus used to measure the oxygen consumption rates of eyes and brains.
Fig. 6
Fig. 6. Details of the method used to attach an enucleated eye to a pinhead.
(A) Applying glue to pin (B and C) attaching pin to eye (D) using microscissors to puncture and cut through sclera and retina (E) making two more cuts to have eye in three segments (F) applying glue to pin (G and H) attaching sclera to pin (I) removing lens and irrigating (J) setting pin in septum (K) setting septum in respirometry vial.
Fig. 7
Fig. 7. Details of the method used to dissect and attach the brain to a pinhead.
(A) Series of cuts to remove dorsal skull (B) exposed brain (C) excised brain (D) attaching brain to pre-glued pinhead (E) brain set in respirometer.

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